Increasing incidence of Mycoplasma genitalium is driven by people living with HIV and PrEP users

Abstract

Background

Mycoplasma genitalium (MG) is responsible for non-gonococcal urethritis. Our aim is to describe MG positivity rate and incidence in specific populations.

Methods

Retrospective, surveillance study included all samples collected from 2018 to 2022. All samples were tested with Anyplex II STI7 (Seegene). Incidence rate (IR) was calculated, incidence rate ratios (IRRs) were assessed using Poisson regression model.

Results

The study included 13,504 samples belonging to 7,692 individuals. Overall positivity rate was 2.9% (95%CI 2.6–3.2). Subgroups showed significant differences: 13.6% in PrEP users, 5.2% in STI clinic, 4.6% in people living with HIV (PLWH), 1.2% in Gynecology/Obstetrics Department, 0.5% in Fertility clinic, and 0.5% in the “Other” group (p < .001). A significant increasing temporal trend was registered for PLWH. Over a cumulative follow up of 2,554 years, 293 incident infections were registered with an IR of 11.5 per 100PYFU. Departments showed diverse IRs: 7.9 per 100PYFU for PLWH, 30.1 per 100PYFU for PrEP users, 22.7 per 100PYFU for STI clinic. Poisson regression model found a significant increase in incident rates over time in the overall study population driven by PLWH and PrEP users.

Conclusions

MG is uncommon in the general population with stable trends, while PLWH and PrEP users exhibit increasing positivity rate and incidence.

Keywords

Mycoplasma genitalium sexually transmitted infection PrEP HIV

Introduction

Mycoplasma genitalium (MG) was isolated for the first time in 1981 from urethral culture of two men presenting with non-gonococcal urethritis (NGU).¹ It was initially considered to be able to cause disease only to the genitourinary tract, but further studies demonstrated it may also be responsible for proctitis,^2,3 chronic prostatitis,⁴ epididymitis,⁵ cervicitis,⁶ endometritis,⁷ pelvic inflammatory disease,⁸ sexually acquired reactive arthritis,⁹ and ocular infections.¹⁰ Nevertheless, the risk of transmission per coital act has not been determined yet, even though it is expected to be lower than that for Chlamydia trachomatis.¹¹

The prevalence of MG in the general population is generally low (1%–3.3%).¹² On the other hand, MG prevalence in NGU ranges from 10% to 35%,^13,14 thus contributing significantly to the overall burden of disease. Moreover, the epidemiologic importance of MG lays on his widespread antimicrobial resistance. Azithromycin was commonly used to cure MG but macrolide resistance increased from 10.0% before 2010 to 51.4% in 2016–2017.¹⁵ Macrolide resistance is as issue especially for men who have sex with men (MSM) who show levels as high as 87.1%.¹⁶ Consequently, use of fluoroquinolones has increased to compensate azithromycin low susceptibility, but this shift led to a further rise in antibiotic resistance.¹⁷

Available epidemiologic data are based on relatively small cross-sectional studies focusing on specific groups with definite risks of exposure and do not provide information about incidence. Additionally, many studies have been performed decades ago^18–20 and might not be representative of the current epidemiology. Data about people living with HIV (PLWH) and HIV pre-exposure prophylaxis (PrEP) users, that are considered at major risk of sexually transmitted infections (STIs), have not been described in detail. The aims of the present study are: (i) to describe positivity rate — as a prevalence proxy — and incidence of MG over the 2018–2022 period; (ii) to describe epidemiologic trends in specific populations.

Methods

This retrospective, monocentric surveillance study included all samples that were consecutively sent to the Clinical Microbiology laboratory of our tertiary hospital located in Milan, northern Italy, to be tested for bacterial STIs from January 01, 2018, to December 31, 2022. The samples were stratified according to the department of collection (PrEP clinic; STI clinic; PLWH clinic; Gynecology and Obstetrics (G/O) Department; Fertility Clinic). An additional group termed “Other” included samples collected from hospital departments different from the previous five, from diverse hospitals located in the nearby metropolitan region that were unable to test for STIs, and from the outpatient blood drawing department. The type of specimens analyzed was different depending on the Division of collection: G/O Department and Fertility Clinic gathered cervical swabs, and the group “Other” provided urine samples, while PrEP and STI clinics pooled materials from pharyngeal, urogenital, and anorectal sites.²¹ PLWH clinic collected only urine or pooled material according to treating physician’s decision. The frequency of specimen collection was different depending on the clinic they belong to and consequent diverse guidelines and international recommendations. For the PrEP clinic, pooled materials from pharyngeal, urogenital, and anorectal sites were collected quarterly,²² while in PLWH²³ and STI²⁴ clinics collection was every 6 months. Within the Fertility clinic, the screening was undertaken as part of the routine workup²⁵ before undergoing medical fertilization procedures. For G/O Department and the Other group there are no specific schedules for testing and re-testing.

All samples were analyzed with Anyplex II STI7e (Seegene Inc, Seoul, South Korea) this is a multiplex test which looks simultaneously for Chlamydia trachomatis, Neisseria gonorrhea, Mycoplasma genitalium, Mycoplasma hominis, Ureaplasma parvum, Ureaplasma urealyticum, and Trichomonas vaginalis infections. In everyday practice, our Clinical Microbiology laboratory provides the detailed result for any of these seven bacteria for each sample sent for testing. All assays were performed by trained laboratory technicians blinded to clinical information of the enrolled individuals and to the assay results.

Demographic features and laboratory results were retrieved from hospital electronic records.

Descriptive analysis was conducted to characterize the subjects included in the study. Median values and interquartile ranges (IQR) were used to describe continuous variables, while counts and percentages were employed for qualitative variables. The association between variables was assessed using nonparametric statistics (Pearson’s chi-square and Mann-Whitney U tests, as appropriate).

Positivity rate, as a proxy of prevalence, was calculated as the number of individuals who tested positive for MG divided by the number of subjects undergoing STI testing. Repeated tests for the same person within the same year, either positive or negative, were not accounted more than once. The Cochran-Armitage test for trend was used to assess for the presence of an association between the categorical variable positivity rate and the ordinal variable time. Individuals who collected more than one sample were counted to calculate incidence rate (IR) per 100 patients-year of follow up (PYFU) with 95% confidence intervals (95%CI). Person-time incidence rate was determined by taking the total number of new cases of MG infection, while the denominator was the sum of the intervals between the first and the last test performed for each individual. The incidence rate ratios (IRRs) used to estimate change in MG incidence per calendar year and per department of sample collection were calculated using Poisson regression model (crude and adjusted for age).

Two-tailed p-values were calculated and a value <0.05 was considered statistically significant. Data management and analysis were performed using STATA package, version 16.1 (College Station, TX, StataCorp 2019).

The study was conducted according to the Helsinki declaration. Approval by Ethics Committee was required. All data used in the study were previously anonymized by mean of alphanumeric codes, according to the requirements of the Italian Data Protection Code (leg. Decree 196/2003) and by the general authorizations issued by the Data Protection Authority.

Results

The study included 13,504 samples belonging to 7,692 individuals who collected a median of 1 (IQR 1–2) specimens. They were mainly females (61.7%) and born in Italy (75.7%). The median age was 37 (IQR 30–45) years. Table 1 shows demographic features of the study population.

Table 1.

Demographic features of study population.

		Study population (N = 7,692)	Individuals with all negative tests (N = 7,457)	Individuals with at least one positive test (N = 235)	p
Gender, n (%)	Females	4,743 (61.7)	4,713 (63.2)	30 (12.8)	<0.001
	Males	2,888 (37.5)	2,687 (36.0)	201 (85.5)
	TGW	61 (0.8)	57 (0.8)	4 (1.7)
Age, years, median (IQR)		37 (30–45)	37 (30–45)	35 (29–41)	<0.001
Region of origin, n (%)	Italy	5,826 (75.7)	5,645 (75.7)	181 (77.0)	0.124
	Europe	497 (6.5)	488 (6.6)	9 (3.8)
	MENA	342 (4.4)	334 (4.5)	8 (3.4)
	Africa	122 (1.6)	120 (1.6)	2 (0.9)
	Asia	313 (4.1)	306 (4.1)	7 (3.0)
	Latin America	589 (7.7)	561 (7.5)	28 (11.9)
Department of sample collection, n (%)	PLWH	707 (9.2)	650 (8.7)	57 (24.3)	<0.001
	PrEP	511 (6.6)	405 (5.5)	106 (45.1)
	STI	558 (7.3)	525 (7.0)	33 (14.0)
	G/O	723 (9.4)	714 (9.6)	9 (3.8)
	Fertility	287 (3.7)	285 (3.8)	2 (0.9)
	Other	4,906 (63.8)	4,878 (65.4)	28 (11.9)
Concomitant CT infection, n (%)		332 (4.3)	307 (4.1)	25 (10.6)	<0.001
Concomitant NG infection, n (%)		272 (3.5)	250 (3.4)	22 (9.4)	<0.001
Concomitant other ureaplasmas/mycoplasmas infection, n (%)		2,645 (34.4)	2,496 (33.5)	149 (63.4)	<0.001
Number of samples collected, median (IQR)		1 (1–2)	1 (1–1)	5 (2–9)	<0.001

TGW: transgender women; MENA: Middle East and Northern Africa; CT: Chlamydia trachomatis; NG: Neisseria gonorrhoeae; other ureaplasmas/mycoplasmas: Ureaplasma urealyticum, Ureaplasma parvum, and Mycoplasma hominis.

Data about clinical presentation were available only for PLWH, PrEP, and STIs clinics. Thirty-seven samples (15.7%) were collected in presence of anogenital symptoms and tested positive for MG: urethritis was the most common complaint (25, 10.6%) followed by proctitis (7, 3.0%), epididymitis (4, 1.7%), and prostatitis (1, 0.4%). Positive samples collected in presence of symptoms were 9 out of 57 in PLWH clinic (15.8%), 24 out of 106 in PrEP clinic (22.6%), and 4 out of 33 in STI clinic (12.1%).

The overall positivity rate within the study population was 2.9% (95%CI 2.6–3.2): 7.0% (95% CI 6.1–7.9) in men, 0.6% (95% CI 0.4–0.9) in women, and 6.6% (95% CI 1.8–15.9) in transgender women (TGW). The male-to-female ratio was 17.8. Considering the age classes, the positivity rate was highest in the 20–30 years (4.0%, 68/1,697) and 30–40 years (3.5%, 102/2,917) groups, but there were no differences in terms of age class distribution (p = .180). Positivity rate was significantly different among groups: 13.6% in PrEP users (131/967, 95%CI 11.5–15.9), 5.2% in subjects attending the STI clinic (33/637, 95%CI 3.6–7.2), 4.6% in PLWH (75/1,645, 95%CI 3.6–5.7), 1.2% in G/O Department (9/776, 95%CI 0.5–2.2), 0.5% in women attending the Fertility clinic (2/369, 95%CI 0.1–1.9), and 0.5% in the “Other” group (28/5,271, 95%CI 0.4–0.8), p < .001. In the overall population a significant increasing trend from 2018 (1.1%) to 2022 (4.7%) was observed (p < .001). Similarly, PLWH clinic exhibited a significant increase from 3.0% to 6.2% in the same time span (p = .003). PrEP and STI clinics showed higher positivity rates but failed to demonstrate any temporal trend (p = .607 and p = .296, respectively). The other populations maintained stable values around or below 1.0%. Figure 1 shows the Cochran-Armitage tests for trend for the overall population and stratified according to the group of sample collection.

Figure 1.

Positivity rate of MG infection in the overall population and stratified according to department of sample collection and to year of biological material gathering. Cochran-Armitage test for trend was used to assess significant changes over time from 2018 to 2022.

The “Other” category was the largest (4,906 individuals, 63.8%) with a large proportion of women (3,604, 73.5%). The median age was 37 (IQR 31–48) years. Positivity rate was 0.6% (95% CI 0.4–0.8) in the whole group: 0.9% (95% CI 0.5–1.6) in men and 0.4% (95% CI 0.3–0.7) in women. The male-to-female ratio in this group was 2.3. Considering the age classes, the positivity rate was higher in the 20–30 years (1.2%, 12/1,019) and 30–40 years (0.8%, 14/1,761) groups, while was around 0 in the other classes (p = .021). The positivity rate of major bacterial STIs was low (2.3% for Chlamydia trachomatis; 0.8% for gonorrhea), while the other non-pathogenic Ureaplasmas and Mycoplasmas topped to 31.5%.

People that collected more than one sample and entered IR calculation were 1,935. Over a cumulative follow up of 2,554 years, 293 incident infections were registered with an overall IR of 11.5 per 100PYFU (95%CI 10.2–12.8). When considering the different groups, hospital departments showed diverse IRs. Within the PLWH clinic, 89 incident infections were observed over a cumulative follow up of 1,120 years with an IR of 7.9 per 100PYFU (95%CI 6.4–9.7). Within the PrEP clinic, incident cases were 172 with a cumulative follow up of 571 years resulting in an IR of 30.1 per 100PYFU (95%CI 25.9–34.9). The STI clinic enlisted 27 incident infections with a cumulative follow up of 119 years ensuing an IR of 22.7 per 100PYFU (95%CI 15.3–32.6). The other groups had lower incidences. Within the G/O department, 1 infection was observed over a cumulative follow up of 87 years with an IR of 1.2 per 100PYFU (95%CI 0.6–5.7). The “Other” group registered 4 cases over a cumulative follow up of 536 years resulting in an IR of 0.7 per 100PYFU (95%CI 0.2–1.8). None of the women attending the Fertility clinic who collected more than one sample tested positive for MG over a cumulative follow up of 121 years.

The “Other” subpopulation was considered as the reference group within the Poisson regression model this subpopulation because it was characterized by wide age classes and because the other genitourinary STI positivity rates were similar to that found in the general population.^26–28 The Poisson regression model adjusted for age did not find any different incidence for G/O department (p = .142) and Fertility clinic (p = .976), while it was significantly higher for the remaining groups: IRR 8.33 for PLWH (95%CI 5.64–12.30, p < .001), IRR 25.33 for subjects attending the STI clinic (95%CI 17.06–37.61, p < .001), and IRR 18.33 for PrEP users (95%CI 12.51–26.86, p < .001).

A significant increase in incidence rates over time was observed in the overall study population driven by PLWH and PrEP users, while the remaining groups did not show a consistent temporal trend. Generally, there was a slight decrease in 2019, while in 2020 only PrEP users showed an increased IR although at the limit of significance. In 2021 and 2022 the increase was more substantial and statistically significant within PLWH and PrEP clinics. Figure 2 shows IR values fitted over time and Poisson regression models adjusted for age.

Figure 2.

Incident cases of MG infection in the overall population and stratified according to departments of sample collection (only PLWH, PrEP, and STI clinics are shown). Incident rates and fitted values are depicted. Poisson regression model adjusted for age was used to evaluate significant changes in incidence rate over time from 2018 (reference) to 2022.

Discussion

In this study, we estimated the positivity rate of MG infection in a large population of 7,692 individuals and identified groups at increased risk of infection. Among women, the positivity rate intended as a proxy of prevalence was 0.6% (95% CI 0.4–0.9) while in men it was 7.0% (95% CI 6.1–7.9). The infection was more common in the classes from 20 to 50 years of age. Positivity rate and incidence were higher in subjects attending the PLWH and PrEP clinics. These data are consistent with a recent meta-analysis that found a high prevalence of MG in PrEP users compared to non-users (OR 2.30, 95%CI 1.6–3.4).²⁹ Nevertheless, the quality of evidence was very low to moderate. The dynamics registered in these two subgroups depicted a temporal trend from 2018 to 2022 where both positivity rate and incidence increased.

A meta-analysis described a summary prevalence of 1.3% (95%CI 1.0–1.8) in randomly selected samples from the general population (three studies, 9,091 people) in countries with higher levels of development.³⁰ We found a lower positivity rate in the “Other” subpopulation compared to the overall population. Since this group might better describe general unselected people features,^26–28 prevalence of MG might be set to lower percentages (below 1%), with a major involvement of males, and restricted to the 20–40 years age classes. No temporal trends were registered depicting MG as an uncommon, epidemiologically stable pathogen.

No previous study has been able to describe MG incidence. If we consider the “Other” group as representative of the general population, we could estimate incidence at 0.7 per 100PYFU (95%CI 0.2–1.8) with no changes over time. On the other hand, incidence seems much higher in other groups such as individuals attending PLWH, PrEP, and STI clinics where IR ranged from 7.9 to 30.1 per 100PYFU. Additionally, PLWH and PrEP users are the major drivers of an increasing incidence from 2018 to 2022.

This study has several limitations that need to be mentioned. Our study design had a surveillance approach and was based on an evaluation of samples consecutively sent to the Clinical Microbiology laboratory: no data about sexual behavior, use of prophylactic strategies, and exposure to antibiotics could be included in the analysis. Furthermore, information about symptoms could be collected only in PLWH, PrEP, and STI clinics. Importantly, we presented test positivity rates which does not equal clinical disease, as the role of asymptomatic carriage with respect to clinical disease is still unclear. As a consequence, a distinction between recurrent infection, re-infection or persistent infection could not be elucidated: our approach was based on accounting only for one infection those individuals who tested positive more than once in 1 year. This methodology should have minimized this issue. Case accumulation in the PLWH and PrEP clinics and the high male-to-female ratios suggest a major role of MSM at the basis of current MG epidemiology, but no strong conclusions can be drawn. Although our study population was the largest described in the literature, some groups were poorly represented and with different sizes, thus a detailed description of some time frames and within some subpopulations are still limited. The monocentric study design might hamper the generalizability of the results. Pooled materials from pharyngeal, urogenital, and anorectal sites collected in PrEP and STI clinics might have reduced the reliability of diagnostic tests underestimating positivity rate and incidence in these groups. The study period encompassed the COVID-19 pandemic: there were fewer samples collected in 2020 than in the other years and the first general lockdown could have influenced sexual behavior perturbing MG spread.

In conclusion, MG is uncommon in the general population and showed a stable epidemiology over time. On the contrary, PLWH and PrEP users show high positivity rate as a proxy of prevalence and incidence that are increasing in recent years. Since these populations exhibit also extensive levels of antimicrobial resistance, the combined effect of greater spread and low antibiotic susceptibility could represent an epidemiological and clinical threat in the near future. Novel therapeutic approaches and better management information are needed to avoid the development of untreatable STIs in populations at major risks of exposure.

Footnotes

Acknowledgements

The authors wish to thank all subjects who agreed to participate to this study. Preliminary results have been presented as an oral abstract at the 23rd IUSTI World Congress - Victoria Falls (Zimbabwe), September 03–07, 2022.

Author contributions

RR did the literature search and data analysis, conceived the study, and wrote the original draft of the manuscript. RR and NBB collected the data. FDA and EI supervised data collection and analysis and regulatory procedures. NBB, LFR, AR, TB, and MB were treating physicians. AN, DF, and CV handled and supervised laboratory samples management and analyses. MP made intellectual contributions to the concept of the study, supervised the study, validated, and edited the first draft. All authors had full access to all the data in the study and had final responsibility for the decision to submit for publication. All authors attest they meet the ICMJE criteria for authorship.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

Ethical Statement

ORCID iD

Roberto Rossotti

References

Tully

Taylor-Robinson

Rose

, et al. Mycoplasma genitalium, a new species from the human urogenital tract. Int J Syst Bacteriol 1983; 33(2): 387–396. DOI: 10.1099/00207713-33-2-387.

Jensen

. Mycoplasma genitalium infections. Diagnosis, clinical aspects, and pathogenesis. Dan Med Bull 2006; 53(1): 1–27.

Bissessor

Tabrizi

Bradshaw

, et al. The contribution of Mycoplasma genitalium to the aetiology of sexually acquired infectious proctitis in men who have sex with men. Clin Microbiol Infect 2016; 22(3): 260–265. DOI: 10.1016/j.cmi.2015.11.016.

Rossotti

Travi

Bana

, et al. A case of chronic bacterial prostatitis due to Mycoplasma genitalium. Sex Transm Infect 2023; 99(8): 571–573. DOI: 10.1136/sextrans-2023-055935.

Ito

Tsuchiya

Yasuda

, et al. Prevalence of genital mycoplasmas and ureaplasmas in men younger than 40 years-of-age with acute epididymitis. Int J Urol 2012; 19(3): 234–238. DOI: 10.1111/j.1442-2042.2011.02917.x.

Manhart

Critchlow

Holmes

, et al. Mucopurulent cervicitis and Mycoplasma genitalium. J Infect Dis 2003; 187(4): 650–657. DOI: 10.1086/367992.

Cohen

Manhart

Bukusi

, et al. Association between Mycoplasma genitalium and acute endometritis. Lancet Lond Engl 2002; 359(9308): 765–766. DOI: 10.1016/S0140-6736(02)07848-0.

Cohen

Mugo

Astete

, et al. Detection of Mycoplasma genitalium in women with laparoscopically diagnosed acute salpingitis. Sex Transm Infect 2005; 81(6): 463–466. DOI: 10.1136/sti.2005.015701.

Taylor-Robinson

Gilroy

Horowitz

, et al. Mycoplasma genitalium in the joints of two patients with arthritis. Eur J Clin Microbiol Infect Dis 1994; 13(12): 1066–1069. DOI: 10.1007/BF02111830.

10.

Björnelius

Jensen

Lidbrink

. Conjunctivitis associated with Mycoplasma genitalium infection. Clin Infect Dis 2004; 39(7): e67–69. DOI: 10.1086/423809.

11.

Horner

Martin

. Mycoplasma genitalium infection in men. J Infect Dis 2017; 216(suppl_2): S396–S405. DOI: 10.1093/infdis/jix145.

12.

Jensen

Cusini

Gomberg

, et al. 2021 European guideline on the management of Mycoplasma genitalium infections. J Eur Acad Dermatol Venereol. 2022;36(5):641-650. DOI:10.1111/jdv.17972.

13.

Taylor-Robinson

Jensen

. Mycoplasma genitalium: from Chrysalis to multicolored butterfly. Clin Microbiol Rev 2011; 24(3): 498–514. DOI: 10.1128/CMR.00006-11.

14.

Manhart

Gaydos

Taylor

, et al. Characteristics of mycoplasma genitalium urogenital infections in a diverse patient sample from the United States: results from the aptima mycoplasma genitalium evaluation study (AMES). J Clin Microbiol 2020; 58(7): e00165–e00220. DOI: 10.1128/JCM.00165-20.

15.

Kenyon

Manoharan-Basil

. Macrolide consumption and resistance in Mycoplasma genitalium. Lancet Infect Dis 2020; 20(11): 1235–1236. DOI: 10.1016/S1473-3099(20)30727-1.

16.

Durukan

Read

TRH

Murray

, et al. Resistance-guided antimicrobial therapy using doxycycline-moxifloxacin and doxycycline-2.5 g azithromycin for the treatment of mycoplasma genitalium infection: efficacy and tolerability. Clin Infect Dis 2020; 71(6): 1461–1468. DOI: 10.1093/cid/ciz1031.

17.

Machalek

Tao

Shilling

, et al. Prevalence of mutations associated with resistance to macrolides and fluoroquinolones in Mycoplasma genitalium: a systematic review and meta-analysis. Lancet Infect Dis 2020; 20(11): 1302–1314. DOI: 10.1016/S1473-3099(20)30154-7.

18.

Andersen

Sokolowski

Østergaard

, et al. Mycoplasma genitalium: prevalence and behavioural risk factors in the general population. Sex Transm Infect 2007; 83(3): 237–241. DOI: 10.1136/sti.2006.022970.

19.

Manhart

Holmes

Hughes

, et al. Mycoplasma genitalium among young adults in the United States: an emerging sexually transmitted infection. Am J Publ Health 2007; 97(6): 1118–1125. DOI: 10.2105/AJPH.2005.074062.

20.

Sonnenberg

Ison

Clifton

, et al. Epidemiology of mycoplasma genitalium in British men and women aged 16–44 years: evidence from the third national survey of sexual attitudes and lifestyles (Natsal-3). Int J Epidemiol 2015; 44(6): 1982–1994. DOI: 10.1093/ije/dyv194.

21.

Durukan

Read

TRH

Bradshaw

, et al. Pooling pharyngeal, anorectal, and urogenital samples for screening asymptomatic men who have sex with men for Chlamydia trachomatis and Neisseria gonorrhoeae. J Clin Microbiol 2020; 58(5): e01969–e011119. DOI: 10.1128/JCM.01969-19.

22.

Brady

Rodger

Asboe

, et al. BHIVA/BASHH guidelines on the use of HIV pre-exposure prophylaxis (PrEP) 2018. HIV Med 2019; 20(Suppl 2): s2–s80. DOI: 10.1111/hiv.12718.

23.

Horberg

Thompson

Agwu

, et al. Primary care guidance for providers of care for persons with human immunodeficiency virus: 2024 update by the HIV medicine association of the infectious diseases society of America. Clin Infect Dis 2024; 12: ciae479. DOI: 10.1093/cid/ciae479.

24.

BASHH British Association for . Sexual health and HIV. Guidance on STI testing, 2021 and 2023, 2023. https://www.bashh.org/resources/40/guidelines_guidance_on_sti_testing_2021_and_2023/.

25.

Lunenfeld

Van Steirteghem

Bertarelli Foundation . Infertility in the third millennium: implications for the individual, family and society: condensed meeting report from the Bertarelli Foundation’s second global conference. Hum Reprod Update 2004; 10(4): 317–326. DOI: 10.1093/humupd/dmh028.

26.

World Health Organization . Chlamydia. Key Facts. https://www.who.int/news-room/fact-sheets/detail/chlamydia.

27.

Kirkcaldy

Weston

Segurado

, et al. Epidemiology of gonorrhoea: a global perspective. Sex Health 2019; 16(5): 401–411. DOI: 10.1071/SH19061.

28.

Cutoiu

Boda

. Prevalence of Ureaplasma urealyticum, Mycoplasma hominis and Chlamydia trachomatis in symptomatic and asymptomatic patients. Biomed Rep 2023; 19(4): 74. DOI: 10.3892/br.2023.1656.

29.

Sokoll

Migliavaca

Siebert

, et al. Prevalence of Mycoplasma genitalium infection among HIV PrEP users: a systematic review and meta-analysis. Sex Transm Infect 2023; 99(5): 351–359. DOI: 10.1136/sextrans-2022-055687.

30.

Baumann

Cina

Egli-Gany

, et al. Prevalence of Mycoplasma genitalium in different population groups: systematic review andmeta-analysis. Sex Transm Infect 2018; 94(4): 255–262. DOI: 10.1136/sextrans-2017-053384.